Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-28T14:47:44.706Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: a review

Published online by Cambridge University Press:  15 February 2013

V. T. S. Rist ,
E. Weiss ,
M. Eklund  and
R. Mosenthin
V. T. S. Rist
Affiliation:
Institute of Animal Nutrition, University of Hohenheim, 70593 Stuttgart, Germany
E. Weiss
Affiliation:
Institute of Animal Nutrition, University of Hohenheim, 70593 Stuttgart, Germany
M. Eklund
Affiliation:
Institute of Animal Nutrition, University of Hohenheim, 70593 Stuttgart, Germany
R. Mosenthin*
Affiliation:
Institute of Animal Nutrition, University of Hohenheim, 70593 Stuttgart, Germany
*
†E-mail: rainer.mosenthin@uni-hohenheim.de
Get access

Abstract

In pigs, the microbial ecosystem of the gastrointestinal tract (GIT) is influenced by various factors; however, variations in diet composition have been identified as one of the most important determinants. Marked changes in fermentation activities and microbial ecology may occur when altering the diet, for example, from milk to solid feed during weaning. In that way, access of pathogens to the disturbed ecosystem is alleviated, leading to infectious diseases and diarrhea. Thus, there is increasing interest in improving intestinal health by use of dietary ingredients suitable to beneficially affect the microbial composition and activity. For example, fermentable carbohydrates have been shown to promote growth of beneficial Lactobacillus species and bifidobacteria, thereby enhancing colonization resistance against potential pathogens or production of short-chain fatty acids, which can be used as energy source for epithelial cells. On the other hand, fermentation of protein results in the production of various potentially toxic products, such as amines and NH3, and is often associated with growth of potential pathogens. In that way, excessive protein intake has been shown to stimulate the growth of potentially pathogenic species such as Clostridium perfringens, and to reduce fecal counts of beneficial bifidobacteria. Therefore, it seems to be a promising approach to support growth and metabolic activity of the beneficial microbiota by developing suitable feeding strategies. For example, a reduction of dietary CP content and, at the same time, dietary supplementation with fermentable carbohydrates have proven to successfully suppress protein fermentation. In addition, the intestinal microbiota seems to be sensible to variations in dietary protein source, such as the use of highly digestible protein sources may reduce growth of protein-fermenting and potentially pathogenic species. The objective of the present review is to assess the impact of dietary protein on microbiota composition and activity in the GIT of piglets. Attention will be given to studies designed to determine the effect of variations in total protein supply, protein source and supplementation of fermentable carbohydrates to the diet on composition and metabolic activity of the intestinal microbiota.

Keywords

intestinal microbiotaprotein fermentationpiglet
Type
Nutrition
Information
animal , Volume 7 , Issue 7 , July 2013 , pp. 1067 - 1078
Copyright
Copyright © The Animal Consortium 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aherne, F, Hogberg, MG, Kornegay, ET, Shurson, GC, Brocksmith, M, Brocksmith, S, Hollis, GR, Pettigrew, JE 1992. Management and nutrition of the newly weaned pig. Pork industry handbook 111. National Pork Producers Council, Des Moines, IA.Google Scholar
Aschenbach, JR, Schwelberger, HG, Ahrens, F, Fürll, B, Gäbel, G 2006. Histamine inactivation in the colon of pigs in relationship to abundance of catabolic enzymes. Scandinavian Journal of Gastroenterology 41, 712–719.CrossRefGoogle ScholarPubMed
Awati, A, Williams, BA, Bosch, MW, Gerrits, WJJ, Verstegen, MWA 2006. Effect of inclusion of fermentable carbohydrates in the diet on fermentation end-product profile in feces of weanling piglets. Journal of Animal Science 84, 2133–2140.Google Scholar
Ball, RO, Aherne, FX 1987. Influence of dietary nutrient density, level of feed intake and weaning age on young pigs. II. Apparent nutrient digestibility and incidence and severity of diarrhea. Canadian Journal of Animal Science 67, 1105–1115.CrossRefGoogle Scholar
Bauer, E, Williams, BA, Smidt, H, Mosenthin, R, Verstegen, MWA 2006. Influence of dietary components on development of the microbiota in single-stomached species. Nutrition Research Reviews 19, 63–78.Google Scholar
Bertschinger, HU, Eggenberger, E, Jucker, H, Pfirter, HP 1979. Evaluation of low nutrient, high fibre diets for the prevention of porcine Escherichia coli enterotoxaemia. Veterinary Microbiology 3, 281–290.Google Scholar
Bikker, P, Dirkzwager, A, Fleddrus, J, Trevis, P, le Huërou-Luron, I, Lallès, JP, Awati, A 2006. The effect of dietary protein and fermentable carbohydrates levels on growth performance and intestinal characteristics in newly weaned piglets. Journal of Animal Science 84, 3337–3345.Google Scholar
Bikker, P, Dirkzwager, A, Fledderus, J, Trevis, P, le Huërou-Luron, I, Lallès, JP, Awati, A 2007. Dietary protein and fermentable carbohydrates contents influence growth performance and intestinal characteristics in newly weaned pigs. Livestock Science 108, 194–197.Google Scholar
Blasco, M, Fondevila, M, Guada, JA 2005. Inclusion of wheat gluten as a protein source in diets for weaned pigs. Animal Research 54, 297–306.Google Scholar
Branner, GR, Böhmer, BM, Erhardt, W, Henke, J, Roth-Maier, DA 2004. Investigation on the precaecal and faecal digestibility of lactulose and inulin and their influence on nutrient digestibility and microbial characteristics. Archives of Animal Nutrition 58, 353–366.Google Scholar
Choct, M, Dersjant-Li, Y, McLeish, J, Peisker, M 2010. Soy oligosaccharides and soluble non-starch polysaccharides: a review of digestion, nutritive and anti-nutritive effects in pigs and poultry. Asian-Australasian Journal of Animal Science 23, 1386–1398.CrossRefGoogle Scholar
Collinder, E, Björnhag, G, Cardona, M, Norin, E, Rehbinder, C, Midtvedt, T 2003. Gastrointestinal host–microbial interactions in mammals and fish: comparative studies in man, mice, rats, pigs, horses, cows, elk, reindeer, salmon and cod. Microbial Ecology in Health and Disease 15, 66–78.Google Scholar
Columbus, D, Cant, JP, de Lange, CFM 2010. Estimating fermentative amino acid losses in the upper gut of pigs. Livestock Science 133, 124–127.Google Scholar
Conway, PL 1994. Function and regulation of the gastrointestinal microbiota of the pig. In Proceedings of the VI International Symposium on Digestive Physiology in Pigs (ed. WB Souffrant and HEAAP Hagemeister), pp. 231–240. FBN Dummerstorf, Germany.Google Scholar
De Lange, CFM, Pluske, J, Gong, J, Nyachoti, CM 2010. Strategic use of feed ingredients and feed additives to stimulate gut health and development in young pigs. Livestock Science 134, 124–134.CrossRefGoogle Scholar
Dongowski, G, Huth, M, Gebhardt, E, Flamme, W 2002. Dietary fiber-rich barley products beneficially affect the intestinal tract of rats. Journal of Nutrition 132, 3704–3714.Google Scholar
Duncan, SH, Louis, P, Flint, HJ 2004. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Applied and Environmental Microbiology 70, 5810–5817.CrossRefGoogle ScholarPubMed
Etheridge, RD, Seerley, RW, Wyatt, RD 1984. The effect of diet on performance, digestibility, blood composition and intestinal microflora of weaned pigs. Journal of Animal Science 58, 1396–1402.CrossRefGoogle ScholarPubMed
Fanning, S, Hall, LJ, Cronin, M, Zomer, A, MacSharry, J, Goulding, D, O'Connell Motherway, M, Shanahan, F, Nally, K, Dougan, G, van Sinderen, D 2012. Bifidobacterial surface-exopolysaccharide facilitates commensal–host interaction through immune modulation and pathogen protection. Proceedings of the National Academy of Sciences 109, 2108–2113.Google Scholar
Gaskins, HR 2001. Intestinal bacteria and their influence on swine growth. In Swine nutrition (ed. AJ Lewis and LL Southern), pp. 585–608. CRC Press LLC, Boca Raton, USA.Google Scholar
Geboes, KP, de Hertogh, G, de Preter, V, Luypaerts, A, Bammens, B, Evenepoel, P, Ghoos, Y, Geboes, K, Rutgeerts, P, Verbeke, K 2006. The influence of inulin on the absorption of nitrogen and the production of metabolites of protein fermentation in the colon. British Journal of Nutrition 96, 1078–1086.Google Scholar
Hampson, DJ 1994. Postweaning Escherichia coli diarrhea in pigs. In Escherichia coli in domestic animals and humans (ed. CL Gyles), pp. 171–191. CAB International, Wallingford, UK.Google Scholar
Heo, JM, Kim, JC, Hansen, CF, Mullan, BP, Hampson, DJ, Pluske, JR 2008. Effects of feeding low protein diets to piglets on plasma urea nitrogen, faecal ammonia nitrogen, the incidence of diarrhea and performance after weaning. Archives of Animal Nutrition 62, 343–358.Google Scholar
Heo, JM, Opapeju, FO, Pluske, JR, Kim, JC, Hampson, DJ, Nyachoti, CM 2012. Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhea without using in-feed antimicrobial compounds. Journal of Animal Physiology and Animal Nutrition . doi: 10.1111/j.1439-0396.2012.01284.x, Published online by Blackwell Verlag 24 March 2012.Google ScholarPubMed
Hermes, RG, Molist, F, Ywazaki, M, Nofrarias, M, Gomez de Segura, A, Gasa, J, Pérez, JF 2009. Effect of dietary level of protein and fiber on the productive performance and health status of piglets. Journal of Animal Science 87, 3569–3577.CrossRefGoogle ScholarPubMed
Hopwood, DE, Hampson, DJ 2003. Interactions between the intestinal microflora, diet and diarrhea, and their influences on the piglet health in the immediate post-weaning period. In Weaning the pig (ed. JR Pluske, JL Dividich and MWA Verstegen), pp. 199–219. Wageningen Academic Publishers, Wageningen, The Netherlands.Google Scholar
Houdijk, JGM, Hartemink, R, Verstegen, MWA, Bosch, MW 2002. Effects of dietary non-digestible oligosaccharides on microbial characteristics of ileal chyme and faeces in weaner pigs. Archives of Animal Nutrition 56, 297–307.Google Scholar
Htoo, JK, Araiza, BA, Sauer, WC, Rademacher, M, Zhang, Y, Cervantes, M, Zijlstra, RT 2007. Effect of dietary protein content on ileal amino acid digestibility, growth performance, and formation of microbial metabolites in ileal and cecal digesta of early-weaned pigs. Journal of Animal Science 85, 3303–3312.Google Scholar
Hughes, R, Magee, EAM, Bingham, S 2000. Protein degradation in the large intestine: relevance to colorectal cancer. Current Issues in Intestinal Microbiology 1, 51–58.Google Scholar
Jeaurond, EA, Rademacher, M, Pluske, JR, Zhu, CH, de Lange, CFM 2008. Impact of feeding fermentable proteins and carbohydrates on growth performance, gut health and gastrointestinal function of newly weaned pigs. Canadian Journal of Animal Science 88, 271–281.Google Scholar
Jensen, BB 1998. The impact of feed additives on the microbial ecology of the gut in young pigs. Journal of Animal and Feed Sciences 7, 45–64.Google Scholar
Jensen, BB 2001. Possible ways of modifying type and amount of products from microbial fermentation in the gut. In Gut environment of pigs (ed. A Piva, KE Bach Knudsen and JE Lindberg), pp. 181–200. Nottingham University Press, Nottingham, UK.Google Scholar
Jensen, BB, Jørgensen, H 1994. Effect of dietary fiber on microbial activity and microbial gas production in various regions of the gastrointestinal tract of pigs. Applied and Environmental Microbiology 60, 1897–1904.CrossRefGoogle ScholarPubMed
Kellogg, TF, Hays, VW, Catron, DV, Quinn, LY, Speer, VC 1964. Effect of level and source of dietary protein on performance and fecal flora of baby pigs. Journal of Animal Science 23, 1089–1094.Google Scholar
Kelly, D, King, TP 2001. Luminal bacteria: regulation of gut function and immunity. In Gut environment of pigs (ed. A Piva, KE Bach Knudsen and JE Lindberg), pp. 113–131. Nottingham University Press, Nottingham, UK.Google Scholar
Kim, JC, Mullan, BP, Hampson, DJ, Pluske, JR 2008. Addition of oat hulls to an extruded rice-based diet for weaner pigs ameliorates the incidence of diarrhoea and reduces indices of protein fermentation in the gastrointestinal tract. British Journal of Nutrition 99, 1217–1225.CrossRefGoogle Scholar
Klose, V, Bayer, K, Bruckbeck, R, Schatzmayr, G, Loibner, A-P 2010. In vitro antagonistic activities of animal intestinal strains against swine-associated pathogens. Veterinary Microbiology 144, 515–521.CrossRefGoogle ScholarPubMed
Kluess, J, Schoenhusen, U, Souffrant, WB, Jones, PH, Miller, BG 2010. Impact of diet composition on ileal digestibility and small intestinal morphology in early-weaned pigs fitted with a T-cannula. Animal 4, 586–594.CrossRefGoogle ScholarPubMed
Konstantinov, SR, Favier, CF, Zhu, WY, Williams, BA, Klüß, J, Souffrant, W-B, de Vos, WM, Akkermans, ADL, Smidt, H 2004. Microbial diversity studies of the porcine gastrointestinal ecosystem during weaning transition. Animal Research 53, 317–324.Google Scholar
Konstantinov, SR, Zhu, WY, Williams, BA, Tamminga, S, de Vos, WM, Akkermans, ADL 2003. Effect of fermentable carbohydrates on piglet faecal bacterial communities as revealed by denaturing gel electrophoresis analysis of 16S ribosomal DNA. FEMS Microbiology Ecology 43, 225–235.Google Scholar
Le Leu, RK, Brown, IL, Hu, Y, Morita, T, Esterman, A, Young, GP 2006. Effect of dietary resistant starch and protein on colonic fermentation and intestinal tumourigenesis in rats. Carcinogenesis 28, 240–245.CrossRefGoogle ScholarPubMed
Li, DF, Nelssen, JL, Reddy, PG, Blecha, F, Hancock, JD, Allee, GL, Goodband, RD, Klemm, RD 1990. Transient hypersensitivity to soybean meal in the early-weaned pig. Journal of Animal Science 68, 1790–1799.Google Scholar
Libao-Mercado, AJ, Zhu, CL, Cant, JP, Lapierre, H, Thibault, J-N, Sève, B, Fuller, MF, de Lange, CFM 2009. Dietary and endogenous amino acids are the main contributors to microbial protein in the upper gut of normally nourished pigs. Journal of Nutrition 139, 1088–1094.Google Scholar
Loh, G, Eberhard, M, Brunner, RM, Hennig, U, Kuhla, S, Kleessen, B, Metges, CC 2006. Inulin alters the intestinal microbiota and short-chain fatty acid concentration in growing pigs regardless of their basal diet. Journal of Nutrition 136, 1198–1202.CrossRefGoogle ScholarPubMed
Lynch, B, Callan, JJ, O'Doherty, JV 2009. The interaction between dietary crude protein and fermentable carbohydrate source on piglet post weaning performance, diet digestibility and selected faecal microbial populations and volatile fatty acid concentration. Livestock Science 124, 93–100.CrossRefGoogle Scholar
Macfarlane, GT, Macfarlane, S 2007. Models for intestinal fermentation: association between food components, delivery systems, bioavailability and functional interactions in the gut. Current Opinion in Biotechnology 18, 156–162.CrossRefGoogle ScholarPubMed
Macfarlane, GT, Gibson, GR, Beatty, E, Cummings, JH 1992. Estimation of short-chain fatty acid production from protein by human intestinal bacteria based on branched-chain fatty acid measurements. FEMS Microbiology Ecology 101, 81–88.Google Scholar
Macfarlane, S, Macfarlane, GT 1995. Proteolysis and amino acid fermentation. In Human colonic bacteria: role in nutrition, physiology and pathology (ed. GR Gibson and GT Macfarlane), pp. 75–100. CRC Press, Boca Raton, Florida, USA.Google Scholar
Manzanilla, EG, Pérez, JF, Martín, M, Blandón, JC, Baucells, F, Kamel, C, Gasa, J 2009. Dietary protein modifies effect of plant extracts in the intestinal ecosystem of the pig at weaning. Journal of Animal Science 87, 2029–2037.CrossRefGoogle ScholarPubMed
Morita, T, Kasaoka, S, Kiriyama, S 2004. Physiological functions of resistant proteins: proteins and peptides regulating large bowel fermentation of indigestible polysaccharide. Journal of AOAC International 87, 792–796.CrossRefGoogle ScholarPubMed
Mosenthin, R, Hambrecht, E, Sauer, WC 1999. Utilisation of different fibres in piglet feeds. In Recent advances in animal nutrition (ed. PC Garnsworthy and J Wiseman), pp. 227–256. Nottingham University Press, Nottingham, UK.Google Scholar
Mosenthin, R, Sauer, WC, Henkel, H, Ahrens, F, de Lange, CF 1992. Tracer studies of urea kinetics in growing pigs: II. The effect of starch infusion at the distal ileum on urea recycling and bacterial nitrogen excretion. Journal of Animal Science 70, 3467–3472.Google Scholar
Nyachoti, CM, Omogbenigun, FO, Rademacher, M, Blank, G 2006. Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low-protein amino acid-supplemented diets. Journal of Animal Science 84, 125–134.Google Scholar
Opapeju, FO, Rademacher, M, Blank, G, Nyachoti, CM 2008. Effect of low-protein amino acid-supplemented diets on the growth performance, gut morphology, organ weights and digesta characteristics of weaned pigs. Animal 2, 1457–1464.CrossRefGoogle ScholarPubMed
Opapeju, FO, Krause, DO, Payne, RL, Rademacher, M, Nyachoti, CM 2009. Effect of dietary protein level on growth performance, indicators of enteric health, and gastrointestinal microbial ecology of weaned pigs induced with postweaning colibacillosis. Journal of Animal Science 87, 2635–2643.Google Scholar
O'Shea, CJ, Lynch, MB, Callan, JJ, O'Doherty, JV 2010. Dietary supplementation with chitosan at high and low crude protein concentrations promotes Enterobacteriaceae in the caecum and colon and increases manure odour emissions from finisher boars. Livestock Science 134, 198–201.Google Scholar
Otto, ER, Yokoyama, M, Hengemuehle, S, von Bermuth, RD, van Kempen, T, Trottier, NL 2003. Ammonia, volatile fatty acids, phenolics, and odor offensiveness in manure from growing pigs fed diets reduced in protein concentration. Journal of Animal Science 81, 1754–1763.Google Scholar
Owusu-Asiedu, A, Nyachoti, CM, Baidoo, SK, Marquardt, RR, Yang, X 2003. Response of early-weaned pigs to an enterotoxigenic Escherichia coli (K88) challenge when fed diets containing spray-dried porcine plasma or pea protein isolate plus egg yolk antibody. Journal of Animal Science 81, 1781–1789.Google Scholar
Partanen, KH, Mroz, Z 1999. Organic acids for performance enhancement in pig diets. Nutrition Research Reviews 12, 117–145.Google Scholar
Paßlack, N, Al-samman, M, Vahjen, W, Männer, K, Zentek, J 2012. Chain length of inulin affects its degradation and the microbiota in the gastrointestinal tract of weaned piglets after a short-term dietary application. Livestock Science 149, 128–136.Google Scholar
Pieper, R, Kröger, S, Richter, JF, Wang, J, Martin, L, Bindelle, J, Htoo, JK, von Smolinski, D, Vahjen, W, Zentek, J, Van Kessel, AG 2012. Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets. Journal of Nutrition 142, 661–667.CrossRefGoogle Scholar
Pietrzak, T, Schad, A, Zentek, J, Mosenthin, R 2002. Biogene Amine in der Tierernährung: Entstehung, Stoffwechsel und physiologische Aspekte. Übersichten zur Tierernährung 31, 37–64.Google Scholar
Pluske, JR, Hampson, D, Williams, IH 1997. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livestock Production Science 51, 215–236.Google Scholar
Pluske, JR, Pethick, DW, Hopwood, DE, Hampson, DJ 2002. Nutritional influences on some major enteric bacterial diseases of pigs. Nutrition Research Reviews 15, 333–371.Google Scholar
Reid, CA, Hillman, K 1999. The effect of retrogradation and amylose/amylopectin ratio of starches on carbohydrate fermentation and microbial populations in the porcine colon. Animal Science 68, 503–510.Google Scholar
Richards, JD, Gong, J, de Lange, CFM 2005. The gastrointestinal microbiota and its role in monogastric nutrition and health with an emphasis on pigs: current understanding, possible modulations, and new technologies for ecological studies. Canadian Journal of Animal Science 85, 421–435.CrossRefGoogle Scholar
Rolfe, R 1997. Colonization resistance. In Gastrointestinal microbiology, vol. 2 gastrointestinal microbes and host interactions (ed. RI Mackie, BA White and RE Isaacson), pp. 501–536. Chapman and Hall, New York, USA.Google Scholar
Roselli, M, Finamore, A, Britti, MS, Konstantinov, SR, Smidt, H, de Vos, WM, Mengheri, E 2007. The novel porcine Lactobacillus sobrius strain protects intestinal cells from enterotoxigenic Escherichia coli K88 infection and prevents membrane barrier damage. Journal of Nutrition 137, 2709–2716.CrossRefGoogle ScholarPubMed
Savage, DC 1977. Microbial ecology of the gastrointestinal tract. Annual Review of Microbiology 31, 107–133.CrossRefGoogle ScholarPubMed
Scott, KP, Gratz, SW, Sheridan, PO, Flint, HJ, Duncan, SH 2012. The influence of diet on the gut microbiota. Pharmacological Research . doi 10.1016/j.phrs.2012.10.020, Published online by Elsevier 09 November 2012.Google Scholar
Stewart, CA, Hillman, K, Maxwell, F, Kelly, D, King, TP 1993. Recent advances in probiosis in pigs: observations on the microbiology of the pig gut. In Recent advances in animal nutrition (ed. PC Gansworthy and DJA Cole), pp. 197–220. Nottingham University Press, Nottingham, UK.Google Scholar
Unger, FM, Viernstein, H 2004. Probiotika: Regenerierende, prophylaktische und adjuvant-therapeutische Anwendungen. Journal für Ernährungsmedizin 6, 24–29.Google Scholar
Ushida, K, Hoshi, S, Ajisaka, K 2002. 13C-NMR studies on lactate metabolism in a porcine gut microbial ecosystem. Microbial Ecology in Health and Disease 14, 241–246.Google Scholar
Van der Waaij, D 1991. The microflora of the gut: recent findings and implications. Digestive Diseases 9, 36–48.Google Scholar
Varel, VH, Yen, JT 1997. Microbial perspective on fiber utilization by swine. Journal of Animal Science 75, 2715–2722.Google Scholar
Wellock, IJ, Fortomaris, PD, Houdijk, JGM, Kyriazakis, I 2006. The effect of dietary protein supply on the performance and risk of post-weaning enteric disorders in newly weaned pigs. Animal Science 82, 327–335.Google Scholar
Wellock, IJ, Fortomaris, PD, Houdijk, JGM, Kyriazakis, I 2008a. Effects of dietary protein supply, weaning age and experimental enterotoxigenic Escherichia coli infection on newly weaned pigs: performance. Animal 2, 825–833.CrossRefGoogle ScholarPubMed
Wellock, IJ, Fortomaris, PD, Houdijk, JGM, Kyriazakis, I 2008b. Effects of dietary protein supply, weaning age and experimental enterotoxigenic Escherichia coli infection on newly weaned pigs: health. Animal 2, 834–842.Google Scholar
Wells, JE, Yen, JT, Miller, DN 2005. Impact of dried skim milk in production diets on Lactobacillus and pathogenic bacterial shedding in growing-finishing swine. Journal of Applied Microbiology 99, 400–407.Google Scholar
Williams, BA, Bosch, MW, Awati, A, Konstantinov, SR, Smidt, H, Akkermans, ADL, Verstegen, MWA, Tamminga, S 2005. In vitro assessment of gastrointestinal tract (GIT) fermentation in pigs: fermentable substrates and microbial activity. Animal Research 54, 191–201.CrossRefGoogle Scholar
Willing, BP, Van Kessel, AG 2009. Intestinal microbiota differentially affect brush border enzyme activity and gene expression in the neonatal gnotobiotic pig. Journal of Animal Physiology and Animal Nutrition 93, 586–595.Google Scholar
Windey, K, de Preter, V, Verbeke, K 2012. Relevance of protein fermentation to the gut health. Molecular Nutrition & Food Research 56, 184–196.Google Scholar